Nickel Oxidation States and Spin States of Bioinorganic Complexes

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Nickel Oxidation States and Spin States of Bioinorganic Complexes from Nickel L‑edge X‑ray Absorption and Resonant Inelastic X‑ray Scattering Hongxin Wang,*,†,‡ Sergei M. Butorin,§ Anthony T. Young,∥ and Jinghua Guo*,∥,⊥ †

Department of Chemistry, University of California, Davis, California 95616, United States Physical Biosciences Division, Lawrence Berkeley National Laboratory, Berkeley, California 94720, United States § Department of Physics and Astronomy, Uppsala University, Box 516, SE-751 20 Uppsala, Sweden ∥ Advanced Light Source, Lawrence Berkeley National Laboratory, Berkeley, California 94720, United States ⊥ Department of Chemistry and Biochemistry, University of California at Santa Cruz, Santa Cruz, California 95064, United States ‡

S Supporting Information *

ABSTRACT: Soft X-ray absorption spectroscopy (XAS) and resonant inelastic X-ray scattering (RIXS) have been performed on several nickel-containing bioinorganic complexes. RIXS spectral features are shown to be informative and diagnostic for the different oxidation states (NiII vs NiIII) and spin states (high spin NiII vs low spin NiII) in these bioinorganic systems. In addition to the experimental results, multiplet simulation has also been performed to assist in understanding the observed XAS and RIXS features. These results demonstrate the power and complementarity of RIXS in identifying the electronic states for covalent and biorelevant complexes for the first time and pave the way for potential RIXS application to real biological systems.

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INTRODUCTION

understanding the catalytic mechanisms of NiFe H2ase and other Ni enzymes. A NiII ion has d8 electronic configuration and can have either a high-spin (HS) state, in which two electrons are unpaired with the other six electrons paired (S = 1), or a low-spin (LS) state, in which all eight electrons are paired (S = 0). Determining the electronic spin state, e.g., whether Ni−R in NiFe H2ase has a LS NiII state or a HS NiII state for its Ni site,2,7,8 is important for Ni enzymology. For simple cases, the Ni spin state can be inferred from the complex’s geometry. For example, a 4-coordinate tetrahedral or a 6-coordinate octahedral complex usually has a small crystal field splitting and a HS NiII site, while a 4-coordinate square planar complex usually has a large crystal field splitting and a LS NiII site, as illustrated in Figure 1. When the two z-ligands in an octahedral coordination are moved away gradually from the metal center, the local environment changes from an octahedral to a square planar symmetry gradually. This causes the d(z2) orbital to first

The wide variety of nickel (Ni) oxidation states (from −1 to +4), local geometries (4-coordinate tetrahedral and square planar, 5-coordinate trigonal bipyramidal and square pyramidal, 6-coordinate octahedral, etc.), and a broad biological relevance make Ni complexes important in chemistry and biochemistry.1 Among the broad variety of oxidation states, NiII and NiIII are the most common and the most important ones in Ni enzymes.1,2 For example, NiFe hydrogenase (H2ase) catalyzes the formation and oxidation of molecular hydrogen and plays a vital role in anaerobic metabolism.3 The as-isolated NiFe H2ase exhibits an active EPR (S = 1/2) signal and has a NiIII site.2,4 Activation with hydrogen gas puts NiFe H2ase into a series of enzymatic states, each differing by one electron reduction.4 Starting from the as-isolated form, these states are called Ni−A, Ni−SI, Ni−C, and Ni−R, with Ni−R having the lowest chemical potential. Since these NiFe H2ase redox states have an alternating EPR signal pattern of active → silent → active → silent, there are numerous proposals for their Ni oxidation states, including NiIII → NiII → NiIII → NiII.2,5,6 Determining the Ni oxidation states, especially NiII vs NiIII, is critical in © 2013 American Chemical Society

Received: March 18, 2013 Revised: October 26, 2013 Published: November 18, 2013 24767

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4],23 was from Collin’s Lab in Carnegie Mellon University. The complex 4 has an innocent and NiIII stabilizing ligand, whose chemical structure is shown in the Supporting Information (Figure S1).23 The samples were prepared inside a nitrogen gas glovebox (with an oxygen level of less than 1 ppm). As all the materials are solids, they were ground into fine powders, as necessary, then evenly spread and pressed onto a piece of UHVcompatible double-sided carbon tape on a sample holder. The as-prepared samples were transferred from the glovebox to the measurement chambers via a sealed sample holder (for XAS measurements) or a sealed vacuum suitcase (for RIXS measurements). Spectral Measurements. XAS spectra were recorded at the Advanced Light Source (ALS) beamline BL4.0.2.26 While the monochromator was scanned across the intended energy region (e.g., 845−890 eV), the total electron yield from the samples was measured using a channeltron electron multiplier. The incident beam intensity was monitored via a gold grid and used as I0 to normalize the total electron yield signal I1. For comparison, the normalized (I1/I0) spectra were renormalized to each other’s maximum. The scans were recorded with a step size of 0.1 eV and an integration time of 1 s/pt. The beamline energy resolution was 0.1 eV. Each final spectrum was the sum of four scans from different sample spots. The energy position of the spectral features was calibrated using a NiF2 sample, which has an L3-edge at 852.7 eV.10 Using a similar procedure, additional XAS for complexes 2, 3, and 4 was obtained using photocurrent measurements at BL7.0.1 prior to the RIXS measurements, confirming the stability and suitability of the samples. The L-edge RIXS spectra were measured at ALS BL7.0.1.16,22,27 The beam spot size is 100 μm × 200 μm. The X-ray emission spectrometer, which uses a 5 m grazingincidence grating and a two-dimensional multichannel plate Xray detector, was mounted perpendicular to the incoming beam in the polarization plane to minimize the elastic contribution at near-edge excitations. To match the spectrometer’s resolution for a better signal level, 0.5 eV beam resolution was used in our RIXS measurements. The RIXS was measured at the Ni L3edge with several excitation energies. For comparison of different spectra, the intensities were normalized to each other’s maximum. To minimize the contribution of the self-absorption effect, the incident angle was set at 25° with respect to the sample surface.27 The RIXS energies were also calibrated with NiF2. All the samples (for XAS and RIXS) were measured at room temperature. To minimize the possibility of radiation damage (especially for covalent samples), a defocused beam (about 1 × 1 mm2) was used in the XAS measurement at BL 4.0.2. In addition, the sample spot was changed for every scan (∼15 min.). The sample spot was moved every minute in the RIXS experiment at BL 7.0.1. Spectral Calculation. The calculations were performed using the resonant part of the Kramers−Heisenberg equation within the framework of crystal-field multiplet theory for the HS and LS Ni2+ ion, as described by Thole. Slater integrals and matrix elements of dipole transitions between 3d9 and 2p53d8 configurations were obtained using Cowan’s28 and Butler’s29 codes, respectively, which were modified by Thole. The radial parts of the 3d−3d and 2p−3d Coulomb and exchange multipole interactions (so-called Slater integrals) were scaled down to 80% of their Hartree−Fock values to account for intra-

Figure 1. Schematic energy diagram for octahedral (left) and square planar (right) d8 orbital and electronic configurations.

go below the d(x2−y2) level, then below the d(xy) level, and eventually below the d(zx) and d(zy) levels. During this process, the Ni site will change from a HS state to a LS state. For a 5-coordinate Ni site, a trigonal bipyramidal configuration will have a HS state, while a square pyramidal Ni site will have a LS state. However, the difference between the two geometries is small, and the metal site could have a boundary case between a HS NiII and a LS NiII state.9 As EPR cannot tell between S = 0 and S = 1, identifying them with X-ray spectroscopy becomes one of the remaining options.2 Although powerful,2,10−13 limitations exist when using soft Xray absorption spectroscopy (XAS) alone to study the metal sites inside biological or complicated molecules because of their covalent nature and overlapping spectral features. On the other hand, resonant inelastic X-ray scattering (RIXS) has the ability to excite and investigate different absorption bands selectively.14 In addition, while XAS reflects the density of states (DOS) of the unoccupied 3d orbitals, RIXS reflects the DOS of the occupied 3d orbitals, providing complementary information.14,15 Due to the low fluorescence yield, soft X-ray RIXS experiments have previously been very challenging.16 Recently, however, the technique has undergone a revival due in large part to three factors: (i) construction and operation of high brightness third-generation synchrotron radiation sources; (ii) design and implementation of high performance beamlines; and (iii) development of high-throughput/high-resolution spectrometers.17,18 Soft X-ray RIXS has now been successfully applied to studies of small molecules and solid materials.19−22 In this paper, we selected a series of covalent bioinorganic Ni complexes, [PhTttBu]NiICO (1), (Ph4As)2NiII[S2C2(CF3)2] (3, LS), and macrocyclic tetraamide NiIII complex (4, LS),23 for soft X-ray XAS and RIXS studies. NiIIO (2, HS) is also measured and analyzed as a reference. The complex 1 is a real NiI complex; the complex 4 is a covalent but true LS NiIII complex due to a NiIII stabilizing ligand;23 and finally, 2 vs 3 provides a HS vs LS NiII comparison. As NiII vs NiIII and HS NiII vs LS NiII are the most interesting issues in Ni enzymes,2,7,8 we focus on these two topics for our RIXS study.

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EXPERIMENTAL SECTION Samples. [PhTttBu]NiICO [PhTttBu = phenyltris((tertbuthylthio)methyl)borate] (NiICO or 1 for short)24 was synthesized in Riordon’s Lab at University of Delaware; NiO (2) and the energy calibration sample NiF2 were purchased from Sigma-Aldrich and used as purchased (purity = 99.5%) both are typical HS NiII complexes; (Ph4As)2NiII[S2C2(CF3)2] (3)25 was from the ExxonMobil Research Corporation; and the macrocyclic tetraamide complex [NiIII(η4 − 1)]−, or complex 24768

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single peak feature for the LS NiII (3). This is consistent with a d7 ground state,10 which has one unoccupied 3dx2−y2 orbital and a half-filled 3dxy orbital at different energy levels (Figure 1). On the other hand, in comparison with a HS NiII (e.g., complex 2), which also has a doublet L3, the LS NiIII (3) has a doublet with its maximum intensity on the higher-energy side rather than on the lower-energy side. RIXS Results. To better understand HS vs LS NiII and NiII vs NiIII sites, a set of Ni L3-edge RIXS spectra for 2, 3, and 4 were recorded with excitation at five different energies: 852.7 eV (a), 853.2 eV (b), 854.0 eV (c), 854.6 eV (d), and 855.2 eV (e). The overall RIXS spectra and the corresponding excitation energies (top inset) for these samples are shown in Figure 3.

atomic configuration interaction and hybridization effects. The polarization of incident photons was taken into account in calculations in accordance with experimental geometry used for measurements. The 10Dq refers to the splitting between t2g and eg orbitals in an octahedral symmetry Oh (the Δ in Figure 1). The multiplet calculations described below used the following parameters: 10Dq = 1.6 eV, Ds = 0.0, and Dt = 0.0 for HS NiII ground state, and 10Dq = 4.3 eV, Ds = 0.91 eV, and Dt = 0.47 eV for LS NiII ground state. The calculated XAS are broadened with 0.6 eV fwhm Lorentzian and 0.4 eV fwhm Gaussian to fit the observed spectra. The calculated RIXS spectra are broadened with 1.1 eV fwhm Gaussian to fit the measured spectra.

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RESULTS AND DISCUSSION XAS Results. XAS spectra for the series of samples 1 (black), 2 (red), 3 (blue), and 4 (green) are shown in Figure 2.

Figure 2. Ni L-edge XAS spectra for the reference sample NiIIO (2, red) and for Ni bioinorganic complexes 1 (black), 3 (blue), and 4 (green).

The L3 peak positions (and centroids) for these Ni complexes are 851.2 (851.3), 852.7 (853.1), 853.4 (853.4), and 853.9 (853.6) eV, respectively. The L3 resonances shift about 0.8 eV per oxidation state increase. Importantly, there is additional spectral information beyond the chemical shifts. The NiICO complex (1) has a single L3 peak, which is consistent with a d9 configuration because there is only one 3d hole available in NiI. The peak at 856 eV is tentatively assigned to the mixed Ni−CO orbital. It is not surprising for some small ligand features following the L3 main peak, especially for covalent ligands.2,10 The intense CO feature at 856 eV is due to the nature of the strong CO back-bonding and mixing with the 3d metal orbitals.22 This mixed orbital has Ni character and thus is observable with Ni XAS. At L2, the main peak and the Ni−CO peak are closer to each other than those at L3. The LS NiII (3) shows an absorption feature similar to NiICO (main peak), except the absorption peaks (centroids) are higher in energy positions. Although the LS NiII has a d8 configuration, it has only one unfilled orbital level, resulting in a single L3 peak. On the other hand, HS NiII, as exemplified by NiO (2), has two partially filled Ni 3d orbitals, leading to more complicated spectral features. The shoulder at the higher energy side of the L3 has often been used as a diagnostic marker for a HS NiII inside chemical complexes and metalloproteins.2,10,11 A split or broadened L2 line is another spectral feature for HS NiII.2,10,11 The HS vs LS NiII XAS features were well reproduced with the multiplet simulation as shown in Figure S2 (Supporting Information). The complexes 3 and 4 both have a square planar geometry and LS electronic structure. However, a doublet peak at L3 resonance was observed for the LS NiIII (4) in contrast to a

Figure 3. RIXS spectra for NiO (2, red), LS NiII (3, blue), and LS NiIII (4, green), excited at energies a (852.7 eV), b (853.2 eV), c (853.9 eV), d (854.8 eV), and e (855.2 eV) in Ni L-edge XAS spectra at the top inset. The letters CT and N* signify charge transfer transition and normal fluorescence emission, respectively.

The excitation energies coincided with the main L3 absorption peaks and satellite structures present in the XAS. In general, RIXS has three basic categories of transitions:30,31 (i) the elastic peak, or Rayleigh scattering, which is the direct transition back to the ground state (e.g., 2p53d8 → 3d7); (ii) resonant energy loss structures due to d−d and charge-transfer (CT) excitations or Raman scattering; and (iii) normal X-ray emission. The Raman-scattering contributions disperse on the photon energy scale, and their peak positions follow the elastic peaks while the structures due to normal emission do not have major energy shifts at different excitation energies. For NiO excited at 852.7 eV (a), the main L3 RIXS peak is at 851.0 eV, which is 1.7 eV lower than the excitation energy. It is known that NiO has three d−d transitions at about 1.0, 1.8 (or 1.6), and 3.0 eV from previous K-,32 L-,33 and M-31,34 edge Ni RIXS. The 851.0 eV RIXS profile (in Figure 3) is centered at about −1.7 eV and covers all three d−d peaks, although the lowest and highest peaks are weaker and unresolved. When excited at 853.2 eV (0.5 eV higher, at b), the L3 RIXS profile center also moves 0.5 eV higher in energy to 851.5 eV, consistent with a Raman scattering nature. As the excitation 24769

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Comparing the calculated HS NiII (red) and LS-NiII (blue) RIXS spectra in Figure 4, we find: (i) For HS NiII, the L3

energy increases above the resonance (to position c, d, and e in Figure 3), the Raman scattering profile continues to follow the elastic peak. Meanwhile, normal fluorescence at 849.7 eV (indicated with a dash-dot red vertical line and a letter of N*) increases gradually and overwhelms the small Raman peaks at the excitation energy of 855.2 eV, 2.5 eV higher than the L3 absorption resonance. Ishii et al.33 reported their Ni L-edge RIXS on NiO, excited in an extensive energy region of 842−882 eV: that work serves as the foundation for understanding NiO RIXS. Our RIXS produced consistent results at five energies (a → e) around the L3 region (around their excitations energies 4 and 5),34 which serves as a good first step to explore more covalent and more complicated samples, such as the complexes 3 and 4. The LS NiIII (4) was excited at energies a, b, and d corresponding to the lower absorption shoulder and the lower and the higher spectral slopes of the main L3 XAS peak, respectively. As is the case with NiO (2, HS NiII), there is a d− d Raman scattering feature at lower energy, although in this case the shift is 1.1 eV lower than the excitation energy rather then the 1.7 eV with NiO. In addition, the line width for 4 is wider than that for NiO, and the features are not as prominent as those for NiO. In addition to the d−d features, there is a small and broad charge transfer (CT) peak located about 5.7 eV lower than the elastic peak when excited at energies a and b. As the excitation energy increases to d, at least part of the strong peak at 850.3 eV could still be due to the CT intensity. Seeing a charge transfer peak in 4 but not in NiO (2) is understandable because a higher valence and more covalent system could have a stronger metal−ligand charge transfer effect. The charge transfer feature is an important and biorelevant spectroscopic property. LS NiII (3) was excited at energies a, b, and cat and around its L3 main peak (b). The energies d and e are too far from the L3 to excite inelastic scattering and produce mainly normal fluorescence. The excitation at the pre-edge energy (a) shows a broad d−d profile at 850.6 eV, 2.1 eV lower than the excitation energy. Its L3 profile is also broader than NiO (similar with the case for complex 4) and could include buried CT structures. Although the LS NiII (3) does not exhibit distinct multiplet structure, there are still some obvious features. These include: (i) the overall peak profile for a LS NiII (3) is always in the lower-energy side of that for a HS NiIIO (2); (ii) LS NiII (3) has an almost invariant RIXS feature as the excitation energy changes, while HS NiIIO exhibits more variation in its RIXS spectra at the different excitation energies. This is probably due to the very covalent nature of our LS NiII complex.25 A broader line width, higher d−d transition energies, and lower CT transition energies could therefore make the overall features overlap with the normal fluorescence emissions and be almost “invariant” as the excitation energy changes from a to c. The RIXS spectra certainly provide additional features to identify HS NiII vs LS NiII in addition to their XAS spectra. RIXS for HS NiII vs LS NiII. To further the understanding in the difference between HS NiII and LS NiII sites, multiplet calculations28,29 were undertaken. In general, a multiplet calculation, which is intrinsically an atomic program, will not be as quantitative as an ab initio calculation when describing systems with orbital hybridization and state mixing. However, as this calculation includes ligand field parameters, it still helps guide the understanding of the XAS and RIXS spectra. Our calculations, in general, reproduced the above phenomenon in the experimentally observed RIXS spectra.

Figure 4. Calculated XAS (upper panel) and RIXS (lower panel) for HS NiII (red) and LS NiII (blue) in the L3 and L2 region. The RIXS spectra were excited at energies indicated with ↓.

intensity is more evenly scattered, as is the L2 intensity, while the major spectral profile for LS-NiII is centered in one region. Part of the reason could be the covalent nature for most LS species, which makes the d−d, CT, and normal emission overlap. Therefore, RIXS for a HS NiII follows the elastic peak well, while that for a LS-NiII is not sensitive to excitation energies; (ii) HS NiII always has higher energy peaks than LS NiII. And it seems LS NiII has a stronger CT, while HS NiII has a stronger d−d feature; (iii) At L2, the HS NiII intensity has a varying intensity profile in its RIXS when the excitation energy passes the absorption edge, while LS NiII has an almost invariant “single” peak. As this study focuses on the RIXS features, normal emission is not included in the spectral calculation. Nevertheless, these calculated features are still similar with the observed RIXS for HS NiO (2) and LS complex 3, respectively. A direct comparison between the observed and the calculated spectra is made in Figure 5. For NiO (2), there is a reasonable agreement between the observed and the calculated RIXS. In this figure, the right most peaks along the black arrow are the elastic peaks; the red arrow indicates the d−d structures; while the blue arrow denotes the CT features. The lower elastic peak intensities in the observed RIXS are due to the fact that the experiment is designed to minimize the Rayleigh scattering. General agreement is also found between the measured and the calculated RIXS for LS NiII at excitation energies b′ and c′ (higher than L3). Differences for LS NiII RIXS are observed at position a′. For a HS NiII, this energy (a) is at the L3 XAS peak, and there is a well-defined excited state. This is not true for LS NiII as the energy is at the pre-edge position. In recent years, application of soft X-ray RIXS has grown both in and beyond the initially studied systems of small 24770

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AUTHOR INFORMATION

Corresponding Authors

*E-mail: [email protected]. *E-mail: [email protected]. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This research is part of the Advanced Biological Experimental X-ray spectroscopy (ABEX) program, which is supported by the U.S. Department of Energy, Office of Biological and Environmental Research. The research is also supported by the National Institutes of Health (GM-65440 to Dr. Stephen P. Cramer in UC Davis). The work at the ALS is supported by the U.S. Department of Energy under the Contract No. DE-AC0205CH11231. The authors also thank Dr. Cramer in UC Davis for the overall support, Dr. C. G. Riordon in University of Delaware, Dr. Kun Wang in ExxonMobil Research and Engineering Co, and Dr. T. J. Collins in Carnegie Mellon University for providing [PhTttBu]NiICO (1), (Ph4As)2NiII[S2C2(CF3)2] (3), and macrocyclic tetraamide NiIII complex (4) samples.

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Figure 5. Calculated (red) vs observed (black) RIXS for HS NiII (a, b, c, d) and calculated (blue) vs observed (gray) RIXS for LS NiII (a′, b′, c′) at L3.

molecules and solid materials.19−22 For example, the combination of a liquid microjet apparatus with an X-ray emission spectrometer enables the investigation of many new systems, such as hydrogen bonding networks in water, chemical bonding in different solvents, and energy transfer at the metal−solvent interface.35,36 This work has further extended soft X-ray RIXS research to the area of covalent and bioinorganic complexes. Benefitting from numerous previous works on biorelated XAS,2,12,37−41 it will also lead us to a RIXS study on larger and more sophisticated bioinorganic model complexes42,43 or small real metalloenzymes (such as 6KDa rubredoxin44) in the future.

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SUMMARY This work has demonstrated that the combination of XAS and RIXS produces a powerful tool in resolving electronic structures and distinguishing different electronic states, e.g., NiII vs NiIII and HS NiII vs LS NiII sites. In particular, the extension of the RIXS technique to bioinorganic complexes has proven to be very informative. For example, the RIXS spectrum for a LS NiII has a less variable feature and a lower L3 energy position in comparison with that for a HS NiII. These features were reproduced using multiplet theoretical simulations. The RIXS spectra provide additional evidence to determine the electronic spin state for NiII that is complementary to XAS.2,11 LS NiIII RIXS shows a clear charge transfer band, probably due to its higher charge and higher covalency.

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REFERENCES

(1) Lancaster, J. R. The Bioinorganic Chemistry of Nickel; VCH Publishers: New York, 1988; pp 1−28. (2) Wang, H. X.; Ralston, C. Y.; Patil, D. S.; Jones, R. M.; Gu, W.; Verhagen, M.; Cramer, S. P. Nickel L-Edge Soft X-ray Spectroscopy of Nickel-Iron Hydrogenases and Model Compounds - Evidence for High-Spin Nickel(II) in the Active Enzyme. J. Am. Chem. Soc. 2000, 122, 10544−10552. (3) Fontecilla-Camps, J. C. Biological Nickel. Struct. Bonding 1998, 91, 1−30. (4) Bagyinka, C.; Whitehead, J. P.; Maroney, M. J. An X-ray Absorption Spectroscopic Study of Nickel Redox Chemistry in Hydrogenase. J. Am. Chem. Soc. 1993, 115, 3576−3585. (5) Moura, J. J. G.; Teixeira, M.; Moura, I. The Role of Nickel and Iron-Sulfur Centers in the Bioproduction of Hydrogen. Pure. Appl. Chem. 1989, 61, 915−921. (6) Ogata, H.; Lubitz, W.; Higuchi, Y. NiFe Hydrogenases: Structural and Spectroscopic Studies of the Reaction Mechanism. Dalton Trans. 2009, 7577−7587. (7) Albracht, S. P. J. Nickel Hydrogenases - in Search of the Active Site. Biochim. Biophys. Acta, Bioenerg. 1994, 1188, 167−204. (8) Dole, F.; Fournel, A.; Magro, V.; Hatchikian, E. C.; Bertrand, P.; Guigliarelli, B. Nature and Electronic Structure of the Ni-X Dinuclear Center of Desulfovibrio Gigas Hydrogenase. Implications for the Enzymatic Mechanism. Biochemistry 1997, 36, 7847−7854. (9) Gu, W.; Jacquamet, L.; Patil, D. S.; Wang, H. X.; Evans, D. J.; Smith, M. C.; Cramer, S. P. Refinement of the Nickel Site Structure in Desulfovibrio Gigas Hydrogenase Using Range-Extended EXAFS Spectroscopy. J. Inorg. Biochem. 2003, 93, 41−51. (10) Wang, H. X.; Ge, P. H.; Riordan, C. G.; Brooker, S.; Woomer, C. G.; Collins, T.; Cramer, S. P. Integrated X-ray L Absorption Spectra. Counting Holes in Ni Complexes. J. Phys. Chem. B 1998, 102, 8343−8346. (11) Wang, H. X.; Patil, D. S.; Gu, W.; Jacquamet, L.; Friedrich, S.; Funk, T.; Cramer, S. P. L-Edge X-ray Absorption Spectroscopy of Some Ni Enzymes: Probe of Ni Electronic Structure. J. Electron Spectrosc. Relat. Phenom. 2001, 114, 855−863. (12) Wang, H. X.; Peng, G.; Miller, L. M.; Scheuring, E. M.; George, S. J.; Chance, M. R.; Cramer, S. P. Iron L-edge X-ray Absorption Spectroscopy of Myoglobin Complexes and Photolysis Products. J. Am. Chem. Soc. 1997, 119, 4921−4928. (13) Wang, H. X.; Bryant, C.; LeGros, M.; Wang, X.; Cramer, S. P. Fluorescence-Detected X-ray Magnetic Circular Dichroism of Well-

ASSOCIATED CONTENT

S Supporting Information *

Additional figures are in the Supporting Information (S1), with Figure S1 showing the chemical structure of complex 4 (macrocyclic tetraamide NiIII) and Figure S2 showing the calculated vs observed XAS for the HS NiII (2) vs LS NiII (3) pair. This material is available free of charge via the Internet at http://pubs.acs.org. 24771

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The Journal of Physical Chemistry C

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dx.doi.org/10.1021/jp402404b | J. Phys. Chem. C 2013, 117, 24767−24772